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Ptomaphagus parashant Peck and Wynne, new species (Coleoptera: Leiodidae: Cholevinae: Ptomaphagini): The most troglomorphic Cholevine beetle known from western North America

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Ptomaphagus parashant Peck and Wynne, new species, is described from a cave in northwestern Arizona. This is the most cave-modified (troglomorphic) cholevine species known in western North America. Presently, the type locality is the only known location for this new species. We offer management recommendations including annual monitoring to document unauthorized human visitation to this cave and other suggestions to help protect the species from future human disturbance.
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PTOMAPHAGUS PARASHANT PECK AND WYNNE,NEW SPECIES (COLEOPTERA:
LEIODIDAE:CHOLEVINAE:PTOMAPHAGINI): THE MOST TROGLOMORPHIC
CHOLEVINE BEETLE KNOWN FROM WESTERN NORTH AMERICA
STEWART B. PECK
Department of Biology, Carleton University
Ottawa, ON K1S 5B6, CANADA
AND
J. JUDSON WYNNE
Department of Biological Sciences, Colorado Plateau Biodiversity Center, Colorado Plateau
Research Station, Northern Arizona University, Box 5614
Flagstaff, AZ 86011, U.S.A.
ABSTRACT
Ptomaphagus parashant Peck and Wynne, new species, is described from a cave in northwestern Arizona. This
is the most cave-modified (troglomorphic) cholevine species known in western North America. Presently, the type
locality is the only known location for this new species. We offer management recommendations including annual
monitoring to document unauthorized human visitation to this cave and other suggestions to help protect the species
from future human disturbance.
Key Words: leiodid beetle, Grand Canyon-Parashant National Monument, cave-adapted, taxonomy
Leiodid beetles in the genus Ptomaphagus
Hellwig, 1795 (Coleoptera: Leiodidae: Cholevinae:
Ptomaphagini) are rather frequently found in cave
habitats in the USA (but not Canada). At least a
dozen species known from the southeastern USA
are cave-adapted (troglomorphic and troglobitic)
species, occurring in caves from central Kentucky
to northern Alabama and adjacent Georgia (Peck
1973, 1984). Additionally, several other species are
known to favor cave habitats as non-troglomorphic
(troglophilic) species, as well as other moist and
dark habitats such as animal burrows, insect nests,
andleaflitter(e.g., MacKay 1983; Peck and Skelley
2001, Majka and Langor 2008; Hawkes et al.
2013). Most leiodid beetles are habitat generalists
feeding as adults and larvae on certain fungi or
microorganisms associated with decaying organic
matter (e.g., Majka and Langor 2008).
Recent cave studies by one of us (JW) in Grand
Canyon-Parashant National Monument (hereafter
referred to as Parashant National Monument or
PARA) resulted in the discovery of the first fully
cave-adapted (troglomorphic) species of the genus
Ptomaphagus known from outside the southeastern
USA. We take this opportunity to describe it here.
MATERIAL AND METHODS
This study is based on the comparative exami-
nation of specimens of the new species with some
50 specimens of Ptomaphagus inyoensis Peck and
Gnaspini, 1997, Ptomaphagus fisus Horn, 1885,
Ptomaphagus cocytus Peck, 1973, Ptomaphagus
cavernicola Schwarz, 1898, and Ptomaphagus
californicus LeConte, 1853 from the southwestern
USA, deposited in the collections of the Canadian
Museum of Nature Collection of Insects, Aylmer,
PQ, Canada.
JW and colleagues conducted fieldwork at
PARA-1001 cave (Fig. 1) on Parashant National
Monument, Northwestern Arizona from 31 August
through 2 September 2011. They deployed seven
bait stations using three bait types (fresh sweet
potato, chicken liver, and recently cut tree branches
of Juniperus L. (Cupressaceae)) within two areas
(Site 1 and Site 2; Fig. 1) identified as cave deep
zones (see Howarth 1980, 1982). Baits were placed
directly on the ground or within cracks and fissures
in the cave floor. Bait stations were checked twice
(or every 24 hours) and removed. Also, they con-
ducted one 10-minute, 1-m radius direct intuitive
search within each deep zone. Only leiodid beetle
specimens belonging to the new species described
below are reported here.
To make correct species identifications, it was
necessary to examine the aedeagus of male speci-
mens and the spermatheca of females. These
characters are the most useful to suggest relation-
ships of species with some certainty. Both male
and female specimens were dissected after being
309
The Coleopterists Bulletin, 67(3): 309317. 2013.
relaxed and removed from points or a card. Relax-
ing was by immersion for one day in a commercial
household ammonia-based window cleaning solu-
tion. The specimen was then dissected in 70%
ethyl alcohol. The aedeagus or other structure
was examined, dehydrated in anhydrous ethyl
alcohol, and placed in euparal mounting medium
on a small acetate-plastic microslide. External
Fig. 1. Map of PARA-1001 cave with plotted locations for bait sampling and direct intuitive searches. Ptomaphagus
parashant was detected only in the lower level (or Site 2).
THE COLEOPTERISTS BULLETIN 67(3), 2013310
characters were examined with a stereomicroscope
from 10X to 200X magnification. Structures for
illustration were photographed with a digital
camera mounted on a stereomicroscope. Details
were observed with a compound microscope and
then added to outline illustrations made from the
digital photographs. Scanning electron microscope
images were used to further examine both the
eyespot and antennae. We report data as they
appear on the specimen labels.
We used an alpha-numeric coding system
developed by the National Park Service (NPS)
to safeguard the location of both caves and their
resources. We also provide latitude and longitude
coordinates of the general area to keep the pre-
cise location of the cave confidential. Parashant
National Monument headquarters in Saint George,
Utah has the cipher table with cave codes. A copy
of this paper with actual cave names is on file
at both monument headquarters, National Park
Service and the National Cave and Karst Research
Institute, Carlsbad, New Mexico.
Ptomaphagus parashant Peck and Wynne,
new species
(Figs. 24)
Type Specimens. Holotype female and allo-
type male deposited in Canadian Museum of
Nature (CMN), Ottawa, Canada. Type locality:
USA, Arizona, Mohave County, Parashant National
Monument, PARA-1001 cave, N36°39, W113°37.
Type label data: female holotype; 2.ix.2011, J.J.
Wynne, sweet potato bait #4, site 2, deep zone;
and male allotype, same area but chicken liver
bait #1. Our red label states Ptomaphagus
parashant Peck & Wynne, holotype.Paratypes,
all with yellow paratype labels, seven with same
locality data and five from site 2, direct intuitive
searching, and two from sweet potato bait #4
are deposited at the CMN, the Los Angeles
County Museum, California Academy of Sciences,
and the U.S. National Museum of Natural History
(Smithsonian Institution).
Diagnosis. The species is characterized by
its smoothly surfaced and weakly faceted eye
which is reduced to a horizontal diameter of less
than the distance from the front margin of the
eye to the posterior edge of the antennal insertion,
its elongated antennae, the shape of the female
spermatheca, and the different elytral tips of the
two sexes.
Description. Length 3.0 mm from front of
clypeus to tip of elytra. Width 1.2 mm across
widest part of body, about 1/3 of the way down
on the elytra. Color somewhat pale chestnut
brown (Fig. 2). Head finely punctured and pubes-
cent. Eyes reduced, facet remnants only weakly
distinguishable and numbering about 25, eye sur-
face nearly smooth (Fig. 3A-B); eye horizontal
diameter about 0.8 times (range 0.700.85) the
distance from the anterior eye edge to the point
of antennal insertion; eye surface appearing pale
in color (cuticle without pigment) with reflected
light. Antenna (Figs. 3D, 4A) elongate, extend-
ingtofirstquarterofelytrawhenlaidback;
Fig. 2. Ptomaphagus parashant. A) Ventral view, B) Dorsal view, C) Lateral view.
311
THE COLEOPTERISTS BULLETIN 67(3), 2013
THE COLEOPTERISTS BULLETIN 67(3), 2013312
segment III longer than II, segments IV-V similar,
VI shorter, segments VII, IX, and X nearly equal
in length and progressively slightly wider, seg-
ment VIII 3 times wider than long. Pronotum
transversely striate, wider than long, widest at base,
hind angles weakly acuminate. Elytra obliquely
striate, about 4 times longer than broad; female
apex drawn out (Fig. 4C), male hind margin
obliquely truncate, and somewhat drawn out at
tip (Fig. 4D). Wings reduced, variable, no vena-
tion observed; length about 3/5 length of elytra in
some specimens and seemingly absent in others.
Mesosternal notch weakly developed; mesosternal
carina anteriorly nearly flush with mesosternum,
gradually becoming higher to its rounded termi-
nation between middle legs. Legs elongate (Fig. 4B);
male protarsi wider in basal segments than in
female; all male protarsal segments longer than
wide; first male protarsal segment 2.5 times larger
than second and third; metafemur 4.62 times longer
than wide; metatibia 12 times longer than at its
widest; metatarsi all longer than wide, first segment
2.5 times longer than second and third. Aedeagus
typical; parameres ending before aedeagal orifice,
Fig. 3. Ptomaphagus parashant. A) Reflected light image of head with unpigmented remnant eye spot, B) Head
with no eye remnants, C) Dorsal view with elytra open showing no detectable flight wings, D) Antennae; all seg-
ments are actually uniformly pale brown in color in reflected light, yet differences here in illuminationof the apical
flagellomeres are due to differential sputter coating during specimen preparation prior to capturing SEM imagery.
Fig. 4. Ptomaphagus parashant. A) Antenna of allotype male, B) Right metathoracic leg of allotype male, view
of ventral surface, C) Elytral tips of holotype female, D) Elytral tips of paratype male, E) Dorsal surface of aedeagal
tip of paratype male, F) Spermatheca of holotype female. Scale bar = 0.5 mm for A, 1.0 mm for B, C, and D, 0.4 mm
for E, and 0.3 mm for F.
313
THE COLEOPTERISTS BULLETIN 67(3), 2013
with 2 nearly terminal setae; stylet thin, elongate,
gently sinuous; tip (Fig. 4E) in dorsal view gradually
narrowing to apex. Spermatheca (Fig. 4F) with
twisting central shaft, swollen apically and distally,
slight raised crest at anatomically anterior end.
Variation. The only noted variation is in the
size of the eye, which is more reduced in some
specimens than others, and the seemingly variable
state of the reduction of the flight wings (the
elytra were not spread on most specimens to look
for wing remnants).
Etymology. The species name, parashant,is
used as a noun in apposition and was used
because it is the name of the national monu-
ment where this species occurs. This monument
is named for both the Grand Canyon, which is
due south, and Parashant Canyon, which is one
of the major canyons draining into the Colorado
River of the Grand Canyon.
Study Area and Habitat. Located in north-
western Arizona, Grand Canyon-Parashant
National Monument encompasses approximately
4,451 km
2
and occurs at the convergence of
two geological provinces (Basin and Range and
Colorado Plateau). The monument is character-
ized by rugged terrain containing deeply incised
canyons, mesas, and mountains. Vegetation zones
include plants characteristic of the Mojave Desert
at lower elevations, grading through grassland and
juniper shrubland to ponderosa pine forest on
Mt. Trumbull (elevation 2,447 m).
The type locality for this leiodid species is
PARA-1001. This cave is a small solution cave
in the Kaibab limestone and has little secondary
calcite deposition. Its total surveyed length and
depth is 76.2 m and 10.4 m, respectively. The
cave has a small south-facing vertical entrance
in the bottom of a large sinkhole. The cave occurs
within juniper scrublands at 1,585 m elevation.
Specimens of P. parashant were collected from
the lower level (or Site 2; Fig. 1) within the caves
deep (dark) zone. The deep zone environment is
completely dark and characterized by relatively
stable temperature, relatively constant water satu-
rated atmosphere, and often limited to no airflow
(e.g., Howarth 1980, 1982; Howarth and Stone
1990). This cave supports the largest known
camel or cave cricket den (population >1,000
individuals) in Arizona (Wynne, unpublished
data). This population of crickets provides a sig-
nificant nutrient loading into the cave via cricket
guano, cricket eggs and nymphs, as well as
deceased individuals at various life stages. In
other regions, the ecological importance of cave
crickets is well documented (e.g., Barr 1967;
Howarth 1983; Taylor 2003; Culver 2005; Poulson
2005). We suggest it is equally important for both
this ecosystem as well as this new species. Cricket
guano and dead crickets undoubtedly serve as
substrates for the growth of bacteria and fungi
(a food source for leiodid beetles).
Distribution. Ptomaphagus parashant is known
from only one locality in northwestern Arizona
on the north side of the lower Colorado River and
along the western extent of the Grand Canyon. JW
and others have sampled 13 of the largest known
caves in PARA for cavernicolous arthropods
(Wynne, unpublished data); three of these caves
are within a 9.7-km radius of PARA-1001. This
new species was detected in only one cave,
PARA-1001. Given this, we suggest that this new
species represents a narrow-range endemic and
may be endemic to this cave only.
Key to Species. In an earlier key to the spe-
cies of Ptomaphagus (Peck 1973), this spe-
cies fits into a modified couplet 1a: with eyes
unpigmented and greatly reduced (never entirely
absent), with a diameter of less than the dis-
tance between the anterior eye margin and the
edge of the antennal insertion; and being cave-
modified and cave-adapted (a troglobite). This
would lead to couplet 2, which can be modified
as follows:
2a. Troglobites in caves in Mexico .................. 3
2b. Troglobites in caves in the eastern United
States......................................................... 4
2c. Troglobites in caves elsewhere: in NW Arizona
............Ptomaphagus parashant,newspecies
Relationships. Thespermathecaisthestruc-
ture which has proved most useful in suggesting
species relationships in the large genus Ptomaphagus,
with over 60 species in the Nearctic and Neotropi-
cal regions. The shape of the spermatheca (like
areversedSand expanded at both ends)
of P. parashant shows that the species is in the
consobrinus species-group, and not the hirtus or
cavernicola species-groups (Peck 1973). Within the
consobrinus species-group, the spermathecal
morphology is closest to that of the troglophilic
P.fisus in the southwestern U.S. (Peck and Gnaspini
1997). Both this species and troglophilic P. cocytus,
a species with less reduced and clearly faceted eyes
and functional wings from caves in Grand Canyon
National Park (GRCA), have males with a low tooth
on the metafemur, which is lacking in P. parashant.
Other cave inhabiting troglophilic Ptomaphagus
in the southwestern U.S. are P. californicus and
Ptomaphagus inyoensis Peck and Gnaspini, 1997,
but these are less cave-modified and are known
or suspected to occur in non-cave habitats as well.
Also, there are two named, small-eyed, montane,
leaf-litter species in New Mexico, Ptomaphagus
manzano Peck, 1978 and Ptomaphagus lincolnensis
Peck, 1978, but their spermathecae (in curvature
THE COLEOPTERISTS BULLETIN 67(3), 2013314
and terminal swellings) are much less similar.
Additionally, there are several undescribed, small-
eyed, leaf-litter inhabiting species known from
small numbers in the southwestern U.S., especially
the coastal mountains of California, and likely
more remain undiscovered. In conclusion, the rela-
tionships of the species are obscure, but probably
related to an ancestor shared with P. cocytus and
P. fisus, and are clearly not related to any of the
cave species in the mostly eastern hirtus and mostly
Neotropical cavernicola species-groups, all in the
subgenus Adelops Tellk amp f.
It is worth noting that Ptomaphagus, sub-
genus Ptomaphagus, includes about 29 species in
Eurasia, and that only one of these, Ptomaphagus
(Ptomaphagus)troglodytes Blas and Vives, 1983,
is a cave-adapted species known from Grenada,
Spain. Perhaps the great radiation of Leptodirini
(Leiodidae: Cholevinae) in caves of Eurasia some-
how excluded Ptomaphagus from caves there.
DISCUSSION
Peck and Gnaspini (1997) discuss the multiple
cave occupations of various species of Ptomaphagus
in the western U.S. Peck (1980) speculated on the
possible relationships of regional climate change
and alternating periods of inter-glacial aridity as a
driving factor for insects seeking refugia in the
moist habitats of caves in the area of the GRCA
through the Pleistocene.
Ptomaphagus cocytus was described from
four specimens taken from Roaring Springs Cave
in GRCA (Peck 1973) and was evaluated as being
a cave-limited but weakly troglobitic species. The
weak troglomorphisms were its pale yellowish
brown body color, its somewhat reduced but
functional eyes, and the flight wings reduced to
three-quarters the length of the elytra. Later, an
additional 18 specimens were collected from the
type locality cave and six more were found in
Tapeats Cave in GRCA, 50 km to the north by
northwest of Roaring Springs Cave. This new
locality reinforced the supposition that the spe-
cies was a low-level (or relatively unspecialized)
troglobite (Peck 1980).
Recently, another five other specimens were
collected by one of us (JW) from PARA-2202
cave in PARA. These are similar to and presently
identified as P. cocytus. The present conclusion is
they are also separate descendants of a more
widely distributed ancestral species which have
all become isolated as at least three different
cave populations north of the Colorado River in
northwestern Arizona.
Peck (1980) proposed a dynamic and episodic
scenario of sequential isolation of moisture-requiring
arthropods in caves during interglacial arid
periods in the southwestern U.S. He suggested
that P. cocytus and other species at similar stages
of troglomorphy were possibly isolated during
the previous Sangamonian Interglacialsome
125,000 to 80,000 years before present (YBP).
If selective pressures and adaptive rates of mor-
phological change have been comparable, then
we suggest P. parashant represents a time of cave
isolation in a preceding, possibly Yar m o u t h i a n
Interglacialsome 200,000 or more YBP, per-
haps along with a new troglomorphic species of
Tomocerus Nicolet (Collembola: Tomoceridae) from
GRCA caves (Peck 1980).
Management Implications. This is the first
troglomorphic arthropod described from Parashant
National Monument and in northwestern-most
Arizona in general. Currently, this animal is known
from one cave in the region and intensive sam-
pling of this region has not produced this animal
at other locations (Wynne, unpublished data).
Thus, we consider this beetle to be a narrow-range
endemic, and the cave where it occurs should
be managed to ensure the long-term persistence
of the species.
Furthermore, PARA-1001 is one of the most bio-
logically significant caves on the monument. In
addition to this new cave-obligate leiodid beetle,
this cave supports the largest known cave cricket
roost (which also represents an undescribed genus
and species; Wynne, unpublished data) in Arizona,
an undescribed species of troglomorphic centipede
(family Anopsobiidae; Wynne, unpublished data),
and three new species of trogloxenic beetles -
Eleodes wynnei Aalbu, Smith, and Triplehorn
(Tenebrionidae; Aalbu et al. 2012), an undescribed
species of Rhadine LeConte (Carabidae: the
perlevis species-group; T. C. Barr, in litt.), and
an undescribed species of Pterostichus Stephens.
(Carabidae, K. Will, in litt.); to date, the anopsobiid
centipede and Pterostichus sp. have been detected
only in PARA-1001 cave.
Of the numerous anthropogenic impacts known
to negatively affect cave ecosystems, global cli-
mate change (Chevaldonné and Lejeune 2003;
Badino 2004) may pose the most significant threat
to the persistence of this population and to its
habitat in general. Increased aridity and drought
severity is projected for the southwestern U.S.
(e.g., Cayan et al. 2010). Because troglobites are
predominantly stenohygrobic (requiring a near
water-saturated humid atmosphere (Barr and Kuehne
1971; Howarth 1980, 1983)), these projected climate
perturbations may lead to desiccation of the cave
and result in these cave-obligate animals either
retreating deep into any available mesocaverns
(e.g., Howarth 1983) or becoming extinct.
Accordingly, future long-term management and
conservation strategies for this cave should not
315THE COLEOPTERISTS BULLETIN 67(3), 2013
include gating. The caves entrance is on a south-
facing hillside and has a constricted chimney-like
structure. Thus, gating the entrance may alter air
flow (e.g., Elliott 2006), which may result in
accelerating and exacerbating the projected impacts
of global climate change - specifically, direct after-
noon sunlight on a steel or iron gate may result in
the unnatural heating of the cave entrance and ulti-
mate desiccation of the cave.
Given the potential threats, both immediate and
projected, and that this cave supports the highest
richness of cavernicoles on the monument, we
recommend this cave be closed to recreational use.
Additionally, we recommend annual to biennial
population counts (without collecting additional
specimens) applying the same techniques and
same sampling stations (refer to Fig. 1) used to
initially detect P. parashant. Site visits should
include examining the cave and surrounding area
for evidence of human use and intrusion. If evi-
dence of unauthorized human visitation becomes
apparent or problematic (see Wynne 2013 for
more details), then we recommend posting clo-
sure signage at the entrance and/or establishing
other non-invasive management strategies to cur-
tail human use (for more information, refer to
Elliott 2005).
ACKNOWLEDGMENTS
Special thanks are given to Danielle Nelson
and Matt Johnson, Colorado Plateau Research
Station, and Neil Cobb, Colorado Plateau
Museum of Arthropod Biodiversity, for admin-
istrative support. Zach Fitzner, Greg Flores,
Nicholas Glover, and Eathan McIntyre assisted
with fieldwork. San Bernardino Cave Search
and Rescue Team, Jon Jasper and Kyle Voyles,
remained on emergency stand-by during field
operations. The fieldwork component of this
project was recognized as an Explorers Club
Flag Expedition. Caitlin Chapman, Colorado
Plateau Museum of Arthropod Biodiversity,
NAU imaged specimens and Aubrey Funke, Imag-
ing and Histology Core Facility, NAU captured
SEM images of morphological characters. Illus-
trations of morphological characters were pre-
pared by Joyce Cook. Kyle Voyles surveyed
and drafted the map of PARA-1001. F. Génier
and R. Anderson allowed comparative study of
Ptomaphagus specimens under their care in
CMNC. We thank Dale Pate, Eathan McIntyre,
and two anonymous reviewers for providing insight-
ful comments leading to the improvement of this
manuscript. This work was funded through a
Colorado Plateau CESU cooperative agreement
between the National Park Service and Northern
Arizona University.
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THE COLEOPTERISTS BULLETIN 67(3), 2013
... Furthermore, research emphasis should be placed on identifying and surveying nutrient resource sites that support troglomorphic animals ( Howarth et al., 2007;Wynne, 2013;Wynne et al., 2018). For example, Peck & Wynne (2013) showed a cave cricket roost (Family Rhaphidophoridae), within the type locality of the troglomorphic leiodid beetle (Ptomaphagus parashant), provided an important substrate (frass and decaying carcasses) for the growth of fungi -a primary food source for this beetle. ...
... Furthermore, research emphasis should be placed on identifying and surveying nutrient resource sites that support troglomorphic animals ( Howarth et al., 2007;Wynne, 2013;Wynne et al., 2018). For example, Peck & Wynne (2013) showed a cave cricket roost (Family Rhaphidophoridae), within the type locality of the troglomorphic leiodid beetle (Ptomaphagus parashant), provided an important substrate (frass and decaying carcasses) for the growth of fungi -a primary food source for this beetle. Additionally, Stone et al. (2012) and Wynne (2013) underscored the importance of root curtains as both microhabitats and a nutrient source for subterranean-adapted animals in Hawai'i and New Mexico, respectively. ...
... For example, Peck & Wynne (2013) showed a cave cricket roost (Family Rhaphidophoridae), within the type locality of the troglomorphic leiodid beetle (Ptomaphagus parashant), provided an important substrate (frass and decaying carcasses) for the growth of fungi -a primary food source for this beetle. Additionally, Stone et al. (2012) and Wynne (2013) underscored the importance of root curtains as both microhabitats and a nutrient source for subterranean-adapted animals in Hawai'i and New Mexico, respectively. Wynne & Shear (2016), Wynne et al. (2014), andBenedict (1979) identified vegetation and moss within entrances and beneath cave skylights as key habitat for relictual species. ...
Article
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Ever-increasing human pressures on cave biodiversity have amplified the need for systematic, repeatable, and intensive surveys of cave-dwelling arthropods to formulate evidence-based management decisions. We examined 110 papers (from 1967 to 2018) to: (i) understand how cave-dwelling invertebrates have been sampled; (ii) provide a summary of techniques most commonly applied and appropriateness of these techniques, and; (iii) make recommendations for sampling design improvement. Of the studies reviewed, over half (56) were biological inventories, 43 ecologically focused, seven were techniques papers, and four were conservation studies. Nearly one-half (48) of the papers applied systematic techniques. Few papers (24) provided enough information to repeat the study; of these, only 11 studies included cave maps. Most studies (56) used two or more techniques for sampling cave-dwelling invertebrates. Ten studies conducted ≥10 site visits per cave. The use of quantitative techniques was applied in 43 of the studies assessed. More than one-third (42) included some level of discussion on management. Future studies should employ a systematic study design, describe their methods in sufficient detail as to be repeatable, and apply multiple techniques and site visits. This level of effort and detail is required to obtain the most complete inventories, facilitate monitoring of sensitive cave arthropod populations, and make informed decisions regarding the management of cave habitats. We also identified naming inconsistencies of sampling techniques and provide recommendations towards standardization.
... I chose PARA--1001 Cave due to its close proximity to the two hibernacula caves, it is the largest known cricket roost in northern Arizona, and supports the highest diversity of cave--adapted arthropods. It is the only known locality for a troglobitic fungus beetle, Ptomaphagus parashant (Peck & Wynne 2013), two cave--adapted pseudoscorpions endemic to this cave (Harvey and Wynne 2014), and the only known locality for a troglomorphic centipede (family Anopsobiidae, cf Buethobius n. sp.; the first cave--adapted centipede known to Arizona). By studying PARA--1001 Cave, we not only have the ability to compare the climate of a non--hibernacula cave to a hibernacula cave, but we also have the ability to characterize the habitat and microclimate of one of the most biological significant caves on the monument (Peck & Wynne 2013;Wynne and Voyles 2014;Harvey and Wynne 2014). ...
... It is the only known locality for a troglobitic fungus beetle, Ptomaphagus parashant (Peck & Wynne 2013), two cave--adapted pseudoscorpions endemic to this cave (Harvey and Wynne 2014), and the only known locality for a troglomorphic centipede (family Anopsobiidae, cf Buethobius n. sp.; the first cave--adapted centipede known to Arizona). By studying PARA--1001 Cave, we not only have the ability to compare the climate of a non--hibernacula cave to a hibernacula cave, but we also have the ability to characterize the habitat and microclimate of one of the most biological significant caves on the monument (Peck & Wynne 2013;Wynne and Voyles 2014;Harvey and Wynne 2014). ...
Technical Report
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Addressing a knowledge gap concerning the winter ecology of bats on Grand Canyon-‐Parashant National Monument in preparation for the western advance of white-‐nose syndrome (WNS), this paper provides a summary of a three‐year study to estimate population trends of two known cave-roosting bat hibernacula (PARA-0901 and PARA-1401 Caves). Beginning in 2011, we sampled all caves (total 11) likely to support hibernating bats on both Parashant and adjacent BLM lands. Through this effort, colleagues and I identified two hibernacula and three torpor roosts. All but one torpor roost was located on Parashant. The two hibernacula caves became the focus of work in subsequent years (2012 and 2013). Total numbers of hibernating bats ranged from 44 to 51 in PARA­‐0901 Cave, and four to 17 in PARA-­1401 Cave. Most of the bats detected were Corynorhinus townsendii with Myotis sp. infrequently detected in both caves. No visible signs of white­‐nose syndrome (WNS) were observed during the three-year period on either hibernating bats visually examined or in post-­field examination of photographs. Analysis of six sediment samples (with 1 control on surface) from PARA-­0901 Cave tested negative for Pseudogymnoascus destructans (the fungus that causes WNS). In PARA-0901 Cave, the largest hibernaculum, we deployed 41 data loggers and in PARA-­1001 Cave, a non-­hibernaculum cave, we deployed 42 to collect rock surface temperature, ambient temperature, relative humidity and barometric pressure data for two years. For both PARA-0901 and PARA-­1001, we collected 3D cartography data, 3D geospatial data of all microclimatic instrument locations, and 3D geospatial data of all observed hibernating bats. These data will be used to develop models to characterize how microhabitats are selected for hibernation. I will use these models to (a) parameterize habitat requirements of bat hibernacula for at least one cave and (b) simulate climate change effects on this cave to predict whether this roost will become unsuitable for bats at some point in the future. PARA-­1401 Cave was gated in 2009; as a result, the roost is now protected. Presently, PARA-­0901 Cave lacks any safeguards. This cave is the largest known hibernacula on the monument (and in northern Arizona, in general) and is located within one mile of a frequently used cattle tank and corral and is within 300 feet of a single-­track road. To best protect this roost, we recommend this cave be closed to recreational use and the lower chamber ultimately gated. Recommendations are also provided for the establishment of a Western states comprehensive sampling and monitoring strategy of hibernacula for early detection of WNS.
... Onthophagus moroni Zunino and Halffter, 1988 (Scarabaeidae: Scarabaeinae: Onthophagini) is one such species, belonging to the Onthophagus brevifrons species complex of the Onthophagus chevrolati species group, which also includes another four species: Onthophagus cavernicollis Howden and Cartwright, 1963, Onthophagus subtropicus Howden and Cartwright, 1963, Onthophagus brevifrons Horn, 1881 and Onthophagus cuevensis Howden, 1973(Halffter et al. 2019. Onthophagus moroni, O. cavernicollis and O. cuevensis are associated with hypogean environments (e.g., caves) and, because they can spend their entire lives there, are considered troglobites (Giachino and Vailati 2017;Howden and Cartwright 1963;Mammola 2018;Pacheco and Vazde-Mello 2019;Peck and Wynne 2013;Slay et al. 2012;Zunino andHalffter 1988b, 2007). ...
Article
The Onthophagus brevifrons species complex (Coleoptera: Scarabaeidae: Scarabaeinae: Onthophagini) consists of the five species: Onthophagus cavernicollis Howden and Cartwright, Onthophagus subtropicus Howden and Cartwright, Onthophagus brevifrons Horn, Onthophagus cuevensis Howden and Onthophagus moroni Zunino and Halffter, all of which are strictly associated with underground habitats (caves or burrows) and are consequently considered troglobites. Nevertheless, the biology of Onthophagus Latreille species reported from caves is lacking. In this study, four grottoes in the Cuetzalan region were explored: Trompa de Elefante, El Fósil and El Nido del Murciélago (which belong to the poorly explored Gruta de Atepolihui), and the Tasalolpan cave, in the search for dung beetles. Onthophagus moroni was collected inside El Nido del Murciélago and Tasalolpan cave, representing a new record for El Nido del Murciélago, since its presence was previously recorded inside the Tasalolpan cave in 1988. Adults of O. moroni were collected alive 70 m inside the Tasalolpan cave, under a latrine of Peters’ climbing rat, Tylomys nudicaudus (Peters) (Rodentia: Cricetidae). We redescribe the species, discuss its biogeography and provide an updated dichotomous key to enable the identification of the constituent species in the O. brevifrons species complex.
... Cave-adapted species that have reduced eyes (microphthalmy) or are eyeless (anophthalmy) have evolved many times in the family ( Fig. 1) (e.g. Peck 1973, Fresneda et al. 2011, Peck and Wynne 2013. ...
Article
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Small carrion beetles (Coleoptera: Leiodidae: Cholevinae) are members of cave communities around the world and important models for understanding the colonization of caves, adaptation to cave life, and the diversification of cave-adapted lineages. We developed a molecular phylogeny to examine the diversification of the hirtus -group of the small carrion beetle genus Ptomaphagus . The hirtus -group has no surface-dwelling members; it consists of 19 short-range endemic cave- and soil-dwelling species in the central and southeastern United States of America. Taxonomic, phylogenetic and biogeographic data were previously interpreted to suggest the hirtus -group diversified within the past 350,000 years through a series of cave colonization and speciation events related to Pleistocene climate fluctuations. However, our time-calibrated molecular phylogeny resulting from the analysis of 2,300 nucleotides from five genes across three mitochondrial regions ( cox1 , cytb , rrnL - trnL - nad1 ) for all members of the clade paints a different picture. We identify three stages of diversification in the hirtus -group: (1) ~10 million years ago (mya), the lineage that develops into P.shapardi , a soil-dwelling species from the Ozarks, diverged from the lineage that gives rise to the 18 cave-obligate members of the group; (2) between 8.5 mya and 6 mya, seven geographically distinct lineages diverged across Kentucky, Tennessee, Alabama and Georgia; six of these lineages represent a single species today, whereas (3) the ‘South Cumberlands’ lineage in Tennessee and Alabama diversified into 12 species over the past ~6 my. While the events triggering diversification during the first two stages remain to be determined, the distributions, phylogenetic relationships and divergence times in the South Cumberlands lineage are consistent with populations being isolated by vicariant events as the southern Cumberland Plateau eroded and fragmented over millions of years.
... Subterranean Ptomaphagina occur mainly in the Nearctic and Neotropical Regions (Peck 1973(Peck , 1984(Peck , 1998, but the only fully anophthalmic species, Ptomaphagus (Ptomaphagus) troglodytes Blas & Vives, 1983, occurs in Spain, in the Palaearctic Region (Blas and Vives 1983). All Nearctic cave-dwelling species of Ptomaphagina are at most microphthalmic, even the most troglobiomorphic species Ptomaphagus parashant Peck & Wynne, 2013 has remnants of eyes (Peck and Wynne 2013). Microphthalmy in Ptomaphagina has been recently investigated by genetic methods on a population of Ptomaphagus (Adelops) hirtus (Tellkampf, 1844) from the Mammoth cave system in Kentucky, USA (Friedrich et al. 2011;Friedrich 2013). ...
Article
Ptomaphaginustroglodytessp. n. , the first anophthalmic species of Ptomaphaginus Portevin, 1914 is described from two close caves in Libo Karst, south Guizhou Province, China.
... Subterranean Ptomaphagina occur mainly in the Nearctic and Neotropical Regions (Peck 1973(Peck , 1984(Peck , 1998, but the only fully anophthalmic species, Ptomaphagus (Ptomaphagus) troglodytes Blas & Vives, 1983, occurs in Spain, in the Palaearctic Region (Blas and Vives 1983). All Nearctic cave-dwelling species of Ptomaphagina are at most microphthalmic, even the most troglobiomorphic species Ptomaphagus parashant Peck & Wynne, 2013 has remnants of eyes (Peck and Wynne 2013). Microphthalmy in Ptomaphagina has been recently investigated by genetic methods on a population of Ptomaphagus (Adelops) hirtus (Tellkampf, 1844) from the Mammoth cave system in Kentucky, USA (Friedrich et al. 2011;Friedrich 2013). ...
Article
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Ptomaphaginus troglodytes sp. n. , the first anophthalmic species of Ptomaphaginus Portevin, 1914 is described from two close caves in Libo Karst, south Guizhou Province, China.
... Leiodidae are exceptionally successful in the coloni sation of subterranean habitats. Taxa with morphological modifications to subterranean environments (eye and/or wing reduction, depigmentation of the cuticle, etc.) occur in most of the six subfamilies: all species of Catopoceri nae are anophthalmous (PeCk 1975;PeRReau & Růžička 2007;PeCk & Cook 2011); Coloninae: Colon Herbst, 1797 (niSHikawa 2010); Leiodinae: Agathidium (aNGe liNi & De marZo 1986a,b;hoshiNa 2000;hoshiNa et al. 2003;miller & wheeler 2005; ŠVec 2012), Zelodes Leschen, 2000Leschen, (lescheN 2000; Cholevinae: Anemadini: Dissochaetus Reitter, 1885(JeaNNel 1936), Mesocolon Broun, 1911(JeaNNel 1936, Speonemadus Jeannel, 1922(GiachiNo & Vailati 1993, Cholevini: Apterocatops Miyama, 1985(miyama 1985harusawa 2005), Catops Paykull, 1798(PeCk & Cook 2002, Choleva Latreille, 1796 (Růžička & vávRa 2003;borDoNi 2005), Cholevi nus Reitter, 1901(JeaNNel 1936PeRkovSky 1999), Dzun garites Jeannel, 1936(JeaNNel 1936, Rybinskiella Reit ter, 1906(FRank 1988laFer et al. 2001), Eucatopini: Eucatops Portevin, 1903(SzymCzakowSki 1963PeCk & Cook 2005), Leptodirina: all genera except one (JeaNNel 1924), Oritocatopini: Oritocatops Jeannel, 1921(JeaNNel 1964, Ptomaphagini: Adelopsis Portevin, 1907(JeaN Nel 1936, Proptomaphaginus Szymczakowski, 1969(PeCk 1973a, Ptomaphagus Hellwig, 1795, P. (Adelops) Tellkampf, 1844(PeCk 1968, 1973a,b, 1977, 1979PeCk & gnaSPini 1997;PeCk & wynne 2013;FRiedRiCH 2013), P. (Appadelopsis) Gnaspini, 1996(PeCk 1979 and Ptomaphagus s.str. (blas & ViVes 1983;niSHikawa 1993), Ptomaphaginus Szymczakowski, 1969(PeCk 1981, Sciaphyini: Sciaphyes Jeannel, 1910(PeRkovSky 1989hoshiNa & Perreau 2008;FresNeDa et al. 2011). ...
Article
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The “Anemadus smetanai ” species group (Coleoptera: Leiodidae: Cholevinae: Anemadini) is revised. The species group is redefined, including Anemadus smetanai Růžička, 1999, A. kabaki Perreau, 2009 from China: Sichuan province and five new species: A. grebennikovi sp.n. (Yunnan province: Jizu Shan Mts.), A. haba sp.n. (Yunnan province: Haba Xue Shan Mt.), A. hajeki sp.n. (Yunnan province: Cang Shan Mt., Yulong Xue Shan Mts.), A. imurai sp.n. (Sichuan province: Mt. Mianya Shan) and A. tangi sp.n. (Xizang autonomous region: Linzhi county). The species of this group show gradual morphological modifications linked to their endogean life. The conditions of this subterranean evolution and the link with high altitudinal biotopes are discussed. A phylogenetic analysis based on morphological characters is presented. A key for identification of species is provided and the geographical distributions of the seven species are mapped. A new synapomorphy (female genital annulus) is presented. It may provide a significant tool to understand the phylogeny of the Anemadini.
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Subterranean ecosystems are among the most widespread environments on Earth, yet we still have poor knowledge of their biodiversity. To raise awareness of subterranean ecosystems, the essential services they provide, and their unique conservation challenges, 2021 and 2022 were designated International Years of Caves and Karst. As these ecosystems have traditionally been overlooked in global conservation agendas and multilateral agreements, a quantitative assessment of solution-based approaches to safeguard subterranean biota and associated habitats is timely. This assessment allows researchers and practitioners to understand the progress made and research needs in subterranean ecology and management. We conducted a systematic review of peer-reviewed and grey literature focused on subterranean ecosystems globally (terrestrial, freshwater, and saltwater systems), to quantify the available evidence-base for the effectiveness of conservation interventions. We selected 708 publications from the years 1964 to 2021 that discussed, recommended, or implemented 1,954 conservation interventions in subterranean ecosystems. We noted a steep increase in the number of studies from the 2000s while, surprisingly, the proportion of studies quantifying the impact of conservation interventions has steadily and significantly decreased in recent years. The effectiveness of 31% of conservation interventions has been tested statistically. We further highlight that 64% of the reported research occurred in the Palearctic and Nearctic biogeographic regions. Assessments of the effectiveness of conservation interventions were heavily biased towards indirect measures (monitoring and risk assessment), a limited sample of organisms (mostly arthropods and bats), and more accessible systems (terrestrial caves). Our results indicate that most conservation science in the field of subterranean biology does not apply a rigorous quantitative approach, resulting in sparse evidence for the effectiveness of interventions. This raises the important question of how to make conservation efforts more feasible to implement, cost-effective, and long-lasting. Although there is no single remedy, we propose a suite of potential solutions to focus our efforts better towards increasing statistical testing and stress the importance of standardising study reporting to facilitate meta-analytical exercises. We also provide a database summarising the available literature, which will help to build quantitative knowledge about interventions likely to yield the greatest impacts depending upon the subterranean species and habitats of interest. We view this as a starting point to shift away from the widespread tendency of recommending conservation interventions based on anecdotal and expert-based information rather than scientific evidence, without quantitatively testing their effectiveness.
Article
Aim: Identify the optimal combination of sampling techniques to maximize the detection of diversity of cave-dwelling arthropods. Location: Central-western New Mexico; northwestern Arizona; Rapa Nui, Chile. Methods: From 26 caves across three geographically distinct areas in the Western Hemisphere, arthropods were sampled using opportunistic collecting, timed searches, and baited pitfall trapping in all caves, and direct intuitive searches and bait sampling at select caves. To elucidate the techniques or combination of techniques for maximizing sampling completeness and efficiency, we examined our sampling results using nonmetric multidimensional scaling (NMDS), analysis of similarity (ANOSIM), Wilcoxon signed-rank tests, species richness estimators and species accumulation curves. Results: To maximize the detection of cave-dwelling arthropod species, one must apply multiple sampling techniques and specifically sample unique microhabitats. For example, by sampling cave deep zones and nutrient resource sites, we identified several undescribed cave-adapted and/or cave-restricted taxa in the southwestern United States and eight new species of presumed cave-restricted arthropods on Rapa Nui that would otherwise have been missed. Sampling techniques differed in their detection of both management concern species (e.g., newly discovered cave-adapted/restricted species, range expansions of cave-restricted species and newly confirmed alien species) and specific taxonomic groups. Spiders were detected primarily with visual search techniques (direct intuitive searches, opportunistic collecting and timed searches), while most beetles were detected using pitfall traps. Each sampling technique uniquely identified species of management concern further strengthening the importance of a multi-technique sampling approach. Main conclusions: Multiple sampling techniques were required to best characterize cave arthropod diversity. For techniques applied uniformly across all caves, each technique uniquely detected between ~40% and 67% of the total species observed. Also, sampling cave deep zones and nutrient resource sites was critical for both increasing the number of species detected and maximizing the likelihood of detecting management concern species.
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Presented is an annotated catalog of the 38 genera and 382 species of Leiodidae known to occur in the Nearctic Region of North America north of Mexico (the continental USA and Canada). Information on types, distributions, and biologies is included. Twelve of the species also or probably occur in Mexico, and 16 of the species also occur in Europe and/or Asia (i.e., are Holarctic in distribution). Ptomaphagus (Appadelopsis) neojonesi Peck and Newton is proposed as a nomen novum (replacement name) for Ptomaphagus (Adelops) jonesi Peck, 1978, preoccupied by Ptomaphagus valentinei jonesi Jeannel, 1949. Stereus arenarius Peck and Cook, 2009 is transferred to Pseudotriarthron as P. arenarium (Peck and Cook, 2009), new combination.
Technical Report
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I provide a summary of field activities conducted at three caves on 02 February 2013 (0700-1900hr), Grand Canyon-Parashant National Monument, Arizona, USA.
Article
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The cholevine beetles inhabiting burrows of Geomys and Thomomys pocket gophers (Rodentia: Geomyidae) are reviewed. Catops geomysi n. sp. and Ptomaphagus geomysi n. sp. are described. Both of these species and Ptomaphagus schwarzi Hatch appear to be regular and obligate inhabitants of Geomys burrows but are not host specific. Nemadus hornii Hatch, Sciodrepoides ruatsoni hornianus (Blanchard), Catops simplex Say, Ptomaphagus cavernicola Schwarz, Ptomaphagus consobrinus (LeConte), Ptomaphagus fisus Horn, and Ptomaphagus texanus Horn were less frequently collected and are probably facultative inhabitants of Geomys burrows, as well as nests or dens of other small mammals. Ptomaphagus nevadicus Horn is an inhabitant of burrows of Thomomys pocket gophers in western North America. A key to the species of Ptomaphagus in the southeastern Gulf Coastal Plain, from non-cave habitats, is provided to aid in their identification.
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Subgenus Caverneleodes of the genus Eleodes is diagnosed and revised. Six new species from the United States: California (E. microps); Utah and Northern Arizona (E. wynnei), Central Arizona (E. wheeleri), Southern New Mexico (E. quadalupensis), and Mexico (E. thomasi and E. grutus) are described. The biogeography of the subgenus is discussed. Diagnoses and a key are provided to known species of Caverneleodes. Relationships with other Eleodes are discussed. Cave associated Amphidorini are surveyed.
Article
Of the 15 species found, all are terrestrial and 5 are probably now limited to stream caves in the canyon as troglobites or disjunct populations of troglophiles. These 5 species probably descended from forest litter-inhabiting ancestors living near the caves during past glacial-pluvial climates. This 'life zone' lowering occurred most recently from 24 000 to 14 000 yr ago. When the forest retreated upwards at the beginning of the present interglacial (about 8000 yr ago), some of the litter invertebrates which had entered the caves were locally isolated in them when adjacent epigean populations went extinct. -from Author